Ecology Letters, (2011)

doi: 10.1111/j.1461-0248.2010.01578.x

LETTER

A global experiment suggests climate warming will not accelerate litter decomposition in streams but might reduce carbon sequestration

Luz Boyero,1,2* Richard G. Pearson,2 !"

Mark O. Gessner,3,4

Leon A. Barmuta,5

6

Vero´nica Ferreira, Manuel A. S. Grac¸a,6 David Dudgeon,7 Andrew J. Boulton,8 Marcos Callisto,9 Eric Chauvet,10,11 Julie E. Helson,12 Andreas Bruder,3,4 Ricardo J. Albarin˜o,13 Catherine M. Yule,14 Muthukumarasamy Arunachalam,15 Judy N. Davies,8 Ricardo Figueroa,16 Alexander S. Flecker,17 Alonso Ramı´rez,18 Russell G. Death,19 Tomoya Iwata,20 Jude M. Mathooko,21 Catherine Mathuriau,22 Jose´ F. Gonc¸alves Jr,9§ Marcelo S. Moretti,

9–

Tajang Jinggut,

14

Sylvain Lamothe,10,11 Charles

Abstract The decomposition of plant litter is one of the most important ecosystem processes in the biosphere and is particularly sensitive to climate warming. Aquatic ecosystems are well suited to studying warming effects on decomposition because the otherwise confounding influence of moisture is constant. By using a latitudinal temperature gradient in an unprecedented global experiment in streams, we found that climate warming will likely hasten microbial litter decomposition and produce an equivalent decline in detritivore-mediated decomposition rates. As a result, overall decomposition rates should remain unchanged. Nevertheless, the process would be profoundly altered, because the shift in importance from detritivores to microbes in warm climates would likely increase CO2 production and decrease the generation and sequestration of recalcitrant organic particles. In view of recent estimates showing that inland waters are a significant component of the global carbon cycle, this implies consequences for global biogeochemistry and a possible positive climate feedback. Keywords Carbon cycle, climate change, detritivores, global analysis, latitudinal gradient, litter decomposition, microbial decomposers, streams, temperature.

M#Erimba,21 Lavenia Ratnarajah,5 Markus H. Schindler,3 Jose´ Castela,6 Leonardo M. Buria,

13

Ecology Letters (2011)

Aydee´

Cornejo,23,24 Vero´nica D. Villanueva13 and Derek C. West17**

1

Wetland Ecology Department, Don˜ana Biological Station-CSIC, Avda Americo Vespucio s ⁄ n, E-41092 Sevilla, Spain 2 School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia 3 Department of Aquatic Ecology, Eawag: Swiss Federal Institute of Aquatic Science and Technology, U¨berlandstrasse 133, 8600 Du¨bendorf, Switzerland 4 Institute of Integrative Biology, ETH Zu¨rich, Zurich, Switzerland 5 Freshwater Ecology Group, School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania 7001, Australia 6 IMAR-CMA & Department Life Sciences, University of Coimbra, 3001-401 Coimbra, Portugal 7 School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China 8 Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW 2350, Australia 9 Laboratorio de Ecologia de Bentos, Instituto de Cieˆncias Biolo´gicas, Universidade Federal de Minas Gerais, CP 486, 30161-970 Belo Horizonte, MG, Brazil 10 Universite´ de Toulouse, UPS, INPT, EcoLab, 29 rue Jeanne Marvig, F-31055 Toulouse, France 11 CNRS, EcoLab, F-31055 Toulouse, France 12 Surface and Groundwater Ecology Research Group, Department of Biological Sciences, University of Toronto at Scarborough, 1265 Military Trail, Toronto, ON M1C1A4, Canada 13 Laboratorio de Limnologı´a, INIBIOMA, Universidad Nacional del ComahueCONICET, Bariloche, Argentina 14 School of Science, Monash University, Jalan Lagoon Selatan, Bandar Sunway, 46150 Selangor, Malaysia 15 Sri Paramakalyani Centre for Environmental Sciences, Manonmainam Sundaranar University, Alwarkuruchi, Tamil Nadu, India 16 Aquatic Systems Research Unit, Environmental Science Center EULA-Chile, University of Concepcio´n, PO Box 160-C, Concepcio´n, Chile

17

Department of Ecology & Evolutionary Biology, E 203 Corson Hall, Cornell University, Ithaca, NY 14853, USA 18 Institute for Tropical Ecosystem Studies, University of Puerto Rico, PO Box 70377, San Juan, PR 00936, USA 19 Institute of Natural Resources, Ecology PN624, Private Bag 11-222, Palmerston North, New Zealand 20 Faculty of Engineering, University of Yamanashi, 4-3-11 Takeda, Kofu 400-8511, Japan 21 Department of Biological Sciences, Egerton University, PO Box 536, Egerton, Kenya 22 Centro de Investigaciones en Ecosistemas, Antigua Carretera a Pa´tzcuaro No 8701, Ex-Hacienda de San Jose´ de la Huerta, CP 58190, Morelia, Michoaca´n, Mexico 23 Seccio´n de Entomologı´a, Instituto Conmemorativo Gorgas de Estudios de la Salud, Avenida Justo Arosemena & Calle 35, 0816-02593, Panama City, Panama´ 24 Programa Centroamericano de Maestrı´a en Entomologı´a, Universidad de Panama´, Panama City, Panama´ *Correspondence: E-mail: [email protected] !

Present address: Department of Stratified Lakes, Leibniz Institute of Freshwater

Ecology and Inland Fisheries (IGB), Alte Fischerhu¨tte 2, 16775 Stechlin, Germany "

Present address: Department of Ecology, Berlin Institute of Technology

(TU Berlin), Franklinstr. 29, 10587 Berlin, Germany §

Present address: Laborato´rio de Limnologia, Departamento de Ecologia,

IB, Universidade de Brası´lia, 70910-900, Brası´lia, DF, Brazil –

Present address: Centro Universita´rio Vila Velha, Programa de Po´s Graduac¸a˜o

em Ecologia de Ecossistemas, 29102-770, Vila Velha, ES, Brazil **Present address: Department of Ecology & Evolutionary Biology, Yale University, New Haven, CT 06520, USA

! 2011 Blackwell Publishing Ltd/CNRS

2 L. Boyero et al.

INTRODUCTION

Terrestrial plants produce c. 120 billion tons of organic carbon each year (Beer et al. 2010), only a small fraction of which is annually sequestered (Battle et al. 2000) or removed by herbivores (Cebria´n & Duarte 1995). This suggests that the reverse process of plant production – the decomposition of plant litter – is one of the most important ecosystem processes in the biosphere. Therefore, elucidating the spatial patterns and environmental controls of litter decomposition is central to understanding the mechanics of ecosystem functioning both locally and over broad spatial scales. As defined here, litter decomposition involves the biological conversion of dead plant biomass to either CO2 (mineralization) or to other forms of organic matter, such as fine particulate and dissolved organic matter (Seastedt 1984; Gessner et al. 1999), which can then undergo further decomposition. Given the small spatial extent of inland surface waters, most terrestrial plant biomass is decomposed on land. However, recent estimates have shown that decomposition processes in inland waters (Tranvik et al. 2009), including streams and rivers (Battin et al. 2008, 2009), contribute significantly to the global carbon cycle as a result of high metabolic rates, facilitated by constant water availability and nutrient supply, especially in flowing waters. At the same time, plant litter is a pivotal component of stream food webs and ecosystem functioning, particularly in forest systems (Wallace et al. 1997; Gessner et al. 2010). The non-limiting role of water is a key feature that makes aquatic systems a suitable model in which to assess the significance of factors controlling decomposition other than water availability (Lecerf et al. 2007). This is particularly true for temperature, which in terrestrial systems is inextricably linked to moisture as a mutually confounding factor. Aquatic systems are thus particularly valuable when assessing effects of climate warming on decomposition. Climate warming predicted for this century (IPCC 2007) is expected to cause species movements and extinctions, change the composition of communities and alter ecosystem functioning (Mooney et al. 2009). As decomposition depends strongly on temperature (more so than primary production – Davidson & Janssens 2006), it is expected to be particularly sensitive to climate warming. A useful approach to predict ecological effects of climate change is to use latitudinal gradients as surrogates for future temperature changes (Parmesan & Yohe 2003). Assessments of litter decomposition rates over large spatial scales are rare, however, with only one truly global study (Wall et al. 2008), and they are restricted to terrestrial ecosystems, mostly emanating from a single pioneering experiment (Gholz et al. 2000; Parton et al. 2007; Tuomi et al. 2009; Currie et al. 2010). The only aquatic study covering a broad latitudinal gradient was confined to single stream sites in Costa Rica, Michigan and Alaska (Irons et al. 1994). It suggested that microbes are the main determinant of decomposition near the equator, whereas litter-consuming detritivores gain importance at higher latitudes. However, the relative paucity of investigations in the tropics, and particularly the lack of a global-scale dataset, has precluded a robust test of this suggestion (Boyero et al. 2009). Local studies are not coordinated and so differ in their methods, including the use of litter from different plant species that decompose at different rates, thus confounding comparisons of decomposition rates. We overcame these drawbacks in a global decomposition experiment at multiple stream sites on six continents, spanning a latitudinal range from 43" S to 48" N, by using standardized methodology and leaves of a single species. As litter in streams forms discrete patches ! 2011 Blackwell Publishing Ltd/CNRS

Letter

that can be experimentally mimicked and manipulated, decomposition rates and the role of different agents in this process can be quantified. A simple and yet powerful approach to study litter decomposition in the field, widely used in both terrestrial and aquatic systems (Boulton & Boon 1991; Liski et al. 2005), is to measure the mass loss of leaves enclosed in mesh bags, which allow water flow and microbial colonization while excluding detritivores or allowing their access, depending on the mesh size of the bags. Distinction between these two agents of decomposition – microbes and detritivores – is important because their activities are partly governed by different factors and result in varying proportions of decomposition products such as CO2 and dissolved and fine particulate organic matter (Seastedt 1984). Thus, we set out to test, across a broad latitudinal gradient, whether microbial decomposition rates are positively related to temperature (Dang et al. 2009), leading to higher rates in the tropics, and whether the commonly observed dearth of litter consumers in the tropics counters this latitudinal pattern, leading to higher decomposition rates in temperate climates (Irons et al. 1994). MATERIAL AND METHODS

Study sites and field work

Twenty-two study streams were located in both hemispheres and in all inhabited continents (Fig. 1), at absolute latitudes ranging from 0.37" to 47.80" (Table S1). Mean water temperature ranged from 1.9 to 26.0 "C and was strongly related to latitude (y = 24.57 ) 0.38 x; r2 = 0.75; Figure S1). The pH in all streams was circumneutral (7.06 ± 0.18 SE) and conductivity was low (87 lS cm)1 ± 23 SE). The experiment was conducted at the season of maximum leaf litter accumulation, which generally was the dry season at tropical sites and autumn at temperate sites. At each site we chose a single stream reach draining a forested watershed experiencing little human influence. Senescent leaves (c. 3 g) of black alder [Alnus glutinosa (L.) Gaertn.] were air-dried, weighed, enclosed in coarse-mesh (10 mm) and finemesh (0.5 mm) bags and placed in streams. Choice of this species was motivated by the fact that alders are very important riparian species and that they are widely distributed across, and partly beyond, the North Temperate Zone. Importantly, there is also direct experimental evidence showing that alder leaves are highly palatable not only to temperate but also to tropical stream detritivores (Grac¸a et al. 2001).

Figure 1 Location of study sites on six continents (ARG, Argentina; NSW, Australia-New South Wales; QLD, Australia-Queensland; TAS, Australia-Tasmania; BRL, Brazil; CHL, Chile; HKN, China-Hong Kong; CRA, Costa Rica; FRN, France; FGN, French Guiana; GER, Germany; IND, India; JAP, Japan; KEN, Kenya; MLY, Malaysia; MEX, Mexico; NZL, New Zealand; PAN, Panama; PTG, Portugal; PRC, Puerto Rico; TRN, Trinidad; NYK, USA-New York).

Global patterns of decomposition in streams 3

Letter

Three coarse-mesh and three fine-mesh bags were retrieved at each of four dates: day 0 (to determine any weight losses due to handling), and approximately days 14, 28 and 56. Bags were collected with a net (0.5 mm mesh) placed immediately downstream to avoid loss of invertebrates. Leaves were cleaned, oven-dried and weighed. Data analysis

We used linear mixed models (Pinheiro & Bates 2000; Zuur et al. 2009) to test the null hypothesis that decomposition rates do not vary with latitude. To this end, we linearized the simple negative exponential decay model by regressing the natural logarithm of the proportion of litter mass remaining at different sampling dates on the elapsed time (days), latitude of the sampling site (degrees from the equator), elevation (m above sea level), water temperature ("C), mesh size of litter bags (coarse or fine) and the interactions of these factors. To further predict the consequences of climate warming on decomposition rates across latitudes, in a second model we regressed the natural logarithm of the proportion of litter mass remaining on temperature-normalized elapsed time expressed in degree days, latitude, mesh size and their interactions. Degree days were used to normalize for the direct effect of temperature caused by latitude or elevation; they were calculated as time in days multiplied by the average temperature during the experiment, with the threshold set at 0 "C. The slopes of the regression lines were the decay rate coefficient per day or degree day. Models were fitted by generalized least squares (GLS) using restricted maximum likelihood (REML) procedures implemented in R 2.10.0 ($nlme# package for mixed effects modelling: R Development Core Team 2009). Diagnostic plots were inspected to assess deviations from the assumptions of the analysis (Pinheiro & Bates 2000). To account for heterogeneity in variances with increasing time, days or degree days [divided by the maximum value because of the wide range of values (Zuur et al. 2009)] were used as the variance covariate, and a

0.06 0.03 0

(e)

0.12

loge [Decay rate (day–1)]

Decay rate (day–1)

(d)

0.09 0.06 0.03 0 0

5

10 15 20 Water temperature (°C)

25

Patterns across the latitudinal temperature gradient were strikingly different between microbial decomposition in fine-mesh litter bags and combined microbial activity and detritivore feeding in coarsemesh bags (Appendix S1). Microbial decomposition rates clearly increased along the latitudinal temperature gradient (decay rate coefficient of 6.75 · 10)3 at 0 "C with an increase of 1.76 · 10)3 for each "C), notwithstanding considerable scatter across sites (Fig. 2a). Furthermore, when temperature is expressed in the terms of the MTE, then a negative slope results with a coefficient of

(c)

–2

Decay rate (degree-day–1)

0.09

RESULTS AND DISCUSSION

–3 –4 –5 –6 –2 –3 –4 –5 –6

Fine mesh

0.012 0.008 0.004 0

(f) Decay rate (degree-day–1)

(b)

0.12

loge [Decay rate (day–1)]

Decay rate (day–1)

(a)

power transformation of it yielded the lowest Akaike information criterion and satisfactory diagnostic plots of residuals (Pinheiro & Bates 2000; Zuur et al. 2009). Water temperature was also included as a variance covariate in the first model. The need for random terms was established using a likelihood ratio test between the GLS and linear mixed effects model, and the fixed effects were tested by comparing nested models estimated using maximum likelihood and likelihood ratio tests (Zuur et al. 2009). Once the simplest fixed effects structure was found, the final, reduced mixed model was re-fitted with REML and diagnostic plots inspected again (Zuur et al. 2009). Relationships between temperature and decay rate coefficients obtained by the above mixed-model analyses were also explored based on the metabolic theory of ecology (MTE), which provides a framework to assess the relationship between temperature and biological activity in quantitative terms (Gillooly et al. 2001; Brown et al. 2004; Allen et al. 2005). Accordingly, the natural logarithm of the decay rate coefficient was regressed against the inverse of absolute temperature (T) in degrees Kelvin and the Boltzmann constant (k) (Brown et al. 2004). We first used ordinary least-squares regressions but also down-weighted or excluded outliers by means of both robust regressions and the least-trimmed-squares regression procedure implemented in SYSTAT 12 (SYSTAT software, Erkrath, Germany).

39

40 k–1 T–1

41

42

Coarse mesh

0.012 0.008 0.004 0

0

10 20 30 40 Latitude (degrees from equator)

50

Figure 2 Variation in decomposition rates of litter in fine-mesh (a, b, c) and coarse-mesh bags (d, e, f) across 22 globally distributed study sites. Relationships between decomposition coefficients and stream temperature in "C (a, d), between the natural logarithm of decay rate coefficients per day and stream temperature expressed in the terms of metabolic theory of ecology (MTE) as the inverse of absolute temperature (T) in Kelvin and the Boltzmann constant (k) in eV ⁄ k (b, c) and between temperature-normalized decay coefficients per degree day with latitude (e, f). Icons represent a spore of an aquatic fungal decomposer (drawing: E. Chauvet) and a litter-consuming caddisfly larva (drawing: A. Cairns, with permission).

! 2011 Blackwell Publishing Ltd/CNRS

4 L. Boyero et al.

0.46 ± 0.21 (mean ± SE) (Fig. 2b); down-weighting or excluding outliers increases the slope up to 0.58 (robust r2 = 0.40). These estimates compare well with the theoretically expected slope of 0.6– 0.7 (Brown et al. 2004), indicating that the relationship between microbial decomposition rate and temperature also conforms to theory in quantitative terms. This conclusion is supported by the disappearance of the latitudinal gradient in decomposition rates when these are normalized for temperature by applying a degree-day model that assumes that biological activity ceases below the freezing point (Fig. 2c). This normalization results in a common decay rate coefficient of 1.21 · 10)3 per degree day. While the above pattern for microbial decomposition is not unexpected, the distinct latitudinal patterns of decomposition in coarse- and fine-mesh bags indicated that the contribution of detritivores to decomposition was opposite to that of microbes; that is, it was at odds with theory on relationships between temperature and biological activity (Appendix S1). Specifically, regression lines for litter in coarse-mesh bags were flat when decomposition rate coefficients, or their logarithm, were plotted against water temperature (Fig. 2d; common decay rate coefficient of 5.16 · 10)2 per day) or against the inverse of water temperature and the Boltzmann constant (Fig. 2e). In contrast, a significant positive slope emerged when temperature-normalized decay coefficients for litter in coarse-mesh bags were regressed against latitude (Fig. 2f). This was strikingly different from the pattern seen for fine-mesh bags and resulted in a decay rate coefficient of 9.55 · 10)4 per degree day at the equator and an increase by 1.37 · 10)4 per degree day for each degree of latitude north or south. Thus, the observed decline in microbial decomposition rate along the latitudinal temperature gradient was balanced, on average, in coarse-mesh bags. The most parsimonious explanation for this pattern is that litter decomposition mediated by detritivores increases with latitude – whether caused by higher detritivore densities, higher individual feeding capacities related to body size, or a combination of both. In line with this explanation, detritivore densities found in natural leaf packs at half of our study sites (sites for which we have appropriate data, and situated from 41" S to 43" N) increased with latitude (loge detritivore density = 1.36 + 0.10 · latitude, r2 = 0.50, P = 0.015; L. Boyero, R. G. Pearson, R.J. Albarin˜o, M. Callisto, A. Ramı´rez, E. Chauvet, D. Dudgeon, M. Arunachalam, A.J. Boulton, J. Helson & M.A.S. Grac¸a, unpublished data). Our results provide a basis for predicting the effects of climate change on litter decomposition in streams. First, they suggest that microbial decomposition rates in a warmer world can be forecast largely on the basis of projected water temperature. Accordingly, a temperature rise would increase microbial decomposition rates, whose magnitude can be derived from our models. As temperature is projected to rise less near the equator (IPCC 2007), warming could have greater effects on microbial decomposition in temperate areas. Second, it appears that total decomposition rates involving invertebrates are determined by the interplay between water temperature and the occurrence of litter-consuming detritivores, with the balance of these two driving forces resulting in unchanged total decomposition rates in a warmer world. This conclusion is only valid under the premise that climate warming leads to relatively rapid range shifts of detritivores according to the new thermal regimes that establish. There is good reason to believe, based on the current distribution and evolutionary history of litter-consuming detritivores, that poleward retractions will indeed occur in response to climate warming (Parmesan & Yohe 2003). Densities of these detritivores are currently ! 2011 Blackwell Publishing Ltd/CNRS

Letter

higher at higher latitudes (see above) and at higher elevations in the tropics (Yule et al. 2009), suggesting that water temperature plays a major role in their distribution. Moreover, many common litterconsuming detritivores belong to insect orders (Plecoptera, Trichoptera) that evolved in cool waters more than 200 million years ago and are still largely restricted to these cool habitats (Wiggins & Mackay 1978; Balian et al. 2008). Hence, they are unlikely to respond to climate warming by rapid adaptation or acclimatization, and retraction towards higher latitudes and elevations is much more likely. Given the broad geographical scope of our study, factors other than temperature and biogeographical patterns of detritivores likely influenced decomposition rates across sites and accounted for the residual variability around the relationships we found. For example, physical fragmentation or abrasion of decomposing leaves could have contributed to litter mass loss at some of our sites. Importantly, however, such physical effects cannot account for the latitudinal patterns we observed, as there is no plausible mechanism by which fragmentation or abrasion would systematically increase with latitude. If anything, streams would be expected to be flashier (i.e. more disturbance-prone) at lower latitudes because of more intense precipitation events (Boulton et al. 2008), and this would generate a latitudinal pattern opposite to the one we observed. Even that relation is unlikely, however, given that no high-flow events occurred during our field studies, and flume experiments in controlled flow conditions have shown that physical loss of decomposing leaf mass is barely detectable even at quite high current speeds (Ferreira et al. 2006a). Possible differences in dissolved nitrogen concentrations (Ferreira et al. 2006b; Benstead et al. 2009) across streams were also likely to be unimportant in our experiment because we had chosen litter of a nitrogen-fixing plant, black alder, that provides a large nitrogen pool to decomposers, making them independent of nitrogen in the environment. Differences in stream phosphorus concentrations could have played a role (Ardo´n et al. 2006), even though our streams had similar basic characteristics and experienced no or relatively little human influence. Other elements, such as sodium, might also have limited decomposition at some locations, as has recently been shown in terrestrial ecosystems (Kaspari et al. 2009). Variation in these and other factors (e.g. abundance of leaf litter) across sites may well account for some of the residual variability in our decomposition data set. However, the latitudinal patterns we observed emerged regardless, pointing to the robustness of our findings. If, as indicated by our results, climate change produces an increase in microbial decomposition and a concomitant decrease in rates of detritivore-mediated decomposition, then total decomposition rates at a given latitude would remain unchanged in response to climate warming. Nevertheless, climate warming could still have substantial consequences for litter decomposition and the food webs and ecosystems depending on this process because microbial decomposers and detritivores have different effects. In particular, microbial decomposition converts a greater proportion of organic compounds to CO2 (Seastedt 1984; Baldy et al. 2007), whereas detritivores tend to generate large amounts of fine particulate organic matter (Ward et al. 1994) that is more recalcitrant and more easily exported downstream than the parent leaf material. This implies that CO2 production through litter decomposition in streams might increase with climate warming, while the generation of recalcitrant organic particles (Yoshimura et al. 2008) and sequestration in downstream floodplains, lakes or oceans (where environmental conditions are less conducive to decomposition than in streams) could be reduced.

Letter

However, this is only true under the premise that a larger fraction of organic matter than at present is converted to CO2 on an annual basis. Clearly, projections of climate-change effects on litter decomposition would be improved if future global changes in the nature of riparian vegetation and the amounts and quality of litter inputs were known. Conventional models of the global carbon cycle describe inland waters as passive pipes of organic carbon from terrestrial ecosystems to the oceans (Battin et al. 2009). Recent estimates have shown, however, that streams and rivers receive and transform a sizeable fraction of terrestrial net ecosystem production and thus contribute significantly to the global carbon cycle (Battin et al. 2008, 2009). Although this argument is largely based on the turnover of dissolved organic carbon (DOC) received from the watershed, it illustrates the landscape-scale importance of organic matter turnover in stream networks despite their small spatial extent. Plant litter is an important component of organic matter turnover in streams in addition to DOC. Thus, beyond the proof of principle that our study provides, our findings and their implications appear to be directly relevant to global biogeochemistry, with possible positive feedbacks on the climate system (Heimann & Reichstein 2008). ACKNOWLEDGEMENTS

Funded by a grant from the National Geographic Society#s Committee for Research and Exploration [grant number 7980-06; P.I., Luz Boyero; funds went to sites in Latin America (except Puerto Rico), Africa and Asia (except Hong Kong)] and various national funding sources. L. Bre´chet, C. Canhoto, E. Couteau, Z. Dewson, G. Cabarcas, M. Dunfee, B. Gao, Y. Gonza´lez, S. Ha¨ttenschwiler, M. Hirose, D. Hohmann, S. Ka¨ppeli, A. Li, P. Lisle, N. Mochizuki, D. Nawa, L. C. Y. Ng, R. Sa´nchez-Argu¨ello and K. Schmidt helped with field and laboratory work. C. M. Swan and two anonymous referees provided comments on earlier versions of the manuscript. Author contributions: L. B. and R. G. P. conceived the study; L. B. managed the overall project; all authors locally coordinated or performed research; V. F. and M. A. S. G. contributed to data management; L. A. B., L. B., M. O. G. and R. G. P. analysed the data; and L. B., M. O. G., R. G. P. and L. A. B. wrote the paper with input from D. D., V. F., A. J. B., M. A. S. G., M. C., E. C., J. H., A. B., R. J. A., C. M. Y., M. A., J. N. D. and R. F. REFERENCES Allen, A.P., Gillooly, J.F. & Brown, J.H. (2005). Linking the global carbon cycle to individual metabolism. Funct. Ecol., 19, 202–213. Ardo´n, M., Stallcup, L.A. & Pringle, C.M. (2006). Does leaf quality mediate the stimulation of leaf breakdown by phosphorus in Neotropical streams? Freshwat. Biol., 51, 618–633. Baldy, V., Gobert, V., Guerold, F., Chauvet, E., Lambrigot, D. & Charcosset, J.-Y. (2007). Leaf litter breakdown budgets in streams of various trophic status: effects of dissolved inorganic nutrients on microorganisms and invertebrates. Freshwat. Biol., 52, 1322–1335. Balian, E.V., Le´veˆque, C., Segers, H. & Martens, K. (eds) (2008). Freshwater Animal Diversity Assessment (Series: Developments In Hydrobiology, Vol. 198). Springer, New York. Battin, T.J., Kaplan, L.A., Findlay, S., Hopkinson, C.S., Marti, E., Packman, A.I. et al. (2008). Biophysical controls on organic carbon fluxes in fluvial networks. Nat. Geosci., 1, 95–100. Battin, T.J., Luyssaert, S., Kaplan, L.A., Aufdenkampe, A.K., Richter, A. & Tranvik, L.J. (2009). The boundless carbon cycle. Nat. Geosci., 2, 598–600.

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Letter

Yule, C.M., Leong, M.Y., Liew, K.C., Ratnarajah, L., Schmidt, K., Wong, H.M. et al. (2009). Shredders in Malaysia: abundance and richness are higher in cool upland tropical streams. J. N. Am. Benthol. Soc., 28, 404–415. Zuur, A.F., Ieno, E.N., Walker, N., Saveliev, A.A. & Smith, G.M. (2009). Mixed Effects Models and Extensions in Ecology With R. Springer, New York.

SUPPORTING INFORMATION

Additional Supporting Information may be found in the online version of this article: Appendix S1 Supplementary results. Figure S1 Relationship between latitude and mean water temperature

across 22 stream sites distributed on both hemispheres and six continents. Table S1 Location of study sites, site codes, latitude, longitude, elevation and average water temperature. As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be re-organized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Editor, Dag Hessen Manuscript received 19 October 2010 First decision made 17 November 2010 Manuscript accepted 8 December 2010

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